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      Under Cover at Pre-Angiosperm Times: A Cloaked Phasmatodean Insect from the Early Cretaceous Jehol Biota

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          Abstract

          Background

          Fossil species that can be conclusively identified as stem-relatives of stick- and leaf-insects (Phasmatodea) are extremely rare, especially for the Mesozoic era. This dearth in the paleontological record makes assessments on the origin and age of the group problematic and impedes investigations of evolutionary key aspects, such as wing development, sexual size dimorphism and plant mimicry.

          Methodology/Principal Findings

          A new fossil insect species, Cretophasmomima melanogramma Wang, Béthoux and Ren sp. nov., is described on the basis of one female and two male specimens recovered from the Yixian Formation (Early Cretaceous, ca. 126±4 mya; Inner Mongolia, NE China; known as ‘Jehol biota’). The occurrence of a female abdominal operculum and of a characteristic ‘shoulder pad’ in the forewing allows for the interpretation of a true stem-Phasmatodea. In contrast to the situation in extant forms, sexual size dimorphism is only weakly female-biased in this species. The peculiar wing coloration, viz. dark longitudinal veins, suggests that the leaf-shaped plant organ from the contemporaneous ‘gymnosperm’ Membranifolia admirabilis was used as model for crypsis.

          Conclusions/Significance

          As early as in the Early Cretaceous, some stem-Phasmatodea achieved effective leaf mimicry, although additional refinements characteristic of recent forms, such as curved fore femora, were still lacking. The diversification of small-sized arboreal insectivore birds and mammals might have triggered the acquisition of such primary defenses.

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          Most cited references7

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          The evolution of body size: what keeps organisms small?

          It is widely agreed that fecundity selection and sexual selection are the major evolutionary forces that select for larger body size in most organisms. The general, equilibrium view is that selection for large body size is eventually counterbalanced by opposing selective forces. While the evidence for selection favoring larger body size is overwhelming, counterbalancing selection favoring small body size is often masked by the good condition of the larger organism and is therefore less obvious. The suggested costs of large size are: (1) viability costs in juveniles due to long development and/or fast growth; (2) viability costs in adults and juveniles due to predation, parasitism, or starvation because of reduced agility, increased detectability, higher energy requirements, heat stress, and/or intrinsic costs of reproduction; (3) decreased mating success of large males due to reduced agility and/or high energy requirements; and (4) decreased reproductive success of large females and males due to late reproduction. A review of the literature indicates a substantial lack of empirical evidence for these various mechanisms and highlights the need for experimental studies that specifically address the fitness costs of being large at the ecological, physiological, and genetic levels. Specifically, theoretical investigations and comprehensive case studies of particular model species are needed to elucidate whether sporadic selection in time and space is sufficient to counterbalance perpetual and strong selection for large body size.
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            An exceptionally preserved Lower Cretaceous ecosystem.

            Fieldwork in the Early Cretaceous Jehol Group, northeastern China has revealed a plethora of extraordinarily well-preserved fossils that are shaping some of the most contentious debates in palaeontology and evolutionary biology. These discoveries include feathered theropod dinosaurs and early birds, which provide additional, indisputable support for the dinosaurian ancestry of birds, and much new evidence on the evolution of feathers and flight. Specimens of putative basal angiosperms and primitive mammals are clarifying details of the early radiations of these major clades. Detailed soft-tissue preservation of the organisms from the Jehol Biota is providing palaeobiological insights that would not normally be accessible from the fossil record.
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              Ancient pinnate leaf mimesis among lacewings.

              Insects have evolved diverse methods of predator avoidance, many of which implicate complex adaptations of their wings (e.g., Phylliidae, Nymphalidae, Notodontidae). Among these, angiosperm leaf mimicry is one of the most dramatic, although the historical origins of such modifications are unclear owing to a dearth of paleontological records. Here, we report evidence of pinnate leaf mimesis in two lacewings (Neuroptera): Bellinympha filicifolia Y. Wang, Ren, Liu & Engel gen. et sp. nov. and Bellinympha dancei Y. Wang, Ren, Shih & Engel, sp. nov., from the Middle Jurassic, representing a 165-million-year-old specialization between insects and contemporaneous gymnosperms of the Cycadales or Bennettitales. Furthermore, such lacewings demonstrate a preangiosperm origin for leaf mimesis, revealing a lost evolutionary scenario of interactions between insects and gymnosperms. The current fossil record suggests that this enigmatic lineage became extinct during the Early Cretaceous, apparently closely correlated with the decline of Cycadales and Bennettitales at that time, and perhaps owing to the changing floral environment resulted from the rise of flowering plants.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                19 March 2014
                : 9
                : 3
                : e91290
                Affiliations
                [1 ]Key Laboratory of Insect Evolution and Environmental Changes, Capital Normal University, Beijing, P. R. China
                [2 ]Sorbonne Universités - CR2P - MNHN, CNRS, UPMC-Paris6, Paris, France
                [3 ]Johann-Friedrich-Blumenbach-Institute of Zoology and Anthropology, Georg-August-University Göttingen, Göttingen, Germany
                [4 ]Laboratory of Palaeoecology, Xishuangbanna Tropical Botanical Garden, CAS, Menglun, Mengla, Xishuangbanna, Yunnan, P. R. China
                [5 ]Institute of Geology, Department of Palaeontology, Technical University Bergakademie Freiberg, Freiberg, Germany
                USDA-Agricultural Research Service, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Analyzed the data: OB SB. Wrote the paper: MW OB SB FJ YC DR. Supervised the project: DR. Produced the original data: MW OB SB FJ YC.

                Article
                PONE-D-13-41890
                10.1371/journal.pone.0091290
                3960115
                24646906
                8371fa28-752b-41cd-89b7-347d372520c3
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 8 October 2013
                : 13 January 2014
                Page count
                Pages: 10
                Funding
                This research is partly supported by the National Basic Research Program of China (973 Program) (grant 2012CB821906), National Science Foundation of China (grants 31230065, 31272352, 41272006), Project of Great Wall Scholar and KEY project of Beijing Municipal Commission of Education (grants KZ201310028033), China Geological Survey (grant 1212011120115). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Comparative Anatomy
                Ecology
                Evolutionary Ecology
                Paleoecology
                Evolutionary Biology
                Paleontology
                Paleobiology
                Paleozoology
                Invertebrate Paleontology
                Paleobotany
                Taxonomy
                Animal Taxonomy
                Zoology
                Entomology
                Earth Sciences

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